First record of extra-abdominal processes in adult Odonata

2016·1.7 MB·

by  Natalia A. Matushkina

InternationalJournalofOdonatology,2016
Vol.19,Nos.1–2,53–61,http://dx.doi.org/10.1080/13887890.2016.1170732
First record of extra-abdominal processes in adult Odonata
NataliaA.Matushkina∗
DepartmentofZoology,InstituteofBiology,TarasShevchenkoNationalUniversityofKyiv,Kyiv,Ukraine
(Received9October2015;finalversionreceived22March2016)
Pairedextra-abdominalprocesses(ap)werefoundinthepleuralregionofabdominalsegments6–9in
adultOdonataforthefirsttime.Theyareunsegmentedbulge-likeorrod-likestructuresofdifferentsize,
degreeofsclerotizationandmovability.Ashortsearchacrossodonatanfamilieshasshownthatapare
inherentforallstudiedAeshnidaeandforsomeotherAnisoptera.Acomparativestudyoffinalstadium
larvaehasshownthatapappearasremnantsoflarvallateralspinesoriginallysituatedonlarvaltergites.
ThisfactprovidesevidenceaboutthecomplexnatureofthepleuralregionintheAeshnidaeimagowhich
includespartoftheareaofthelarvaltergite.
Keywords: comparative morphology; homology; appendages; abdomen; heterochrony; Odonata;
dragonfly
Introduction
Abdominal appendage-like processes in insects have attracted special interest among scientists
becausetheymayhelpinunderstandingtheearlystagesofinsectevolutionfromanancestorwith
developed abdominal legs (e.g. Bitsch, 2012; Suzuki & Palopoli, 2001). The homology-based
theories of segment transformation in Arthropoda were often based on peculiar morphologi-
cal characters, usually of presumed appendicular origin (e.g. Boxshall,2004, 2013; Giorgianni
& Patel, 2005; Kluge, 1989; Williams & Nagy, 2001). In immature insects, the abdominal
appendageswerestructurallydiverseandmostlyappearedassimpleintegumentaryoutgrowths
like prongs, spines or tubercles, located on the dorsal, lateral or ventral parts of the segments
(see review by Bitsch, 2012). Some of these appendage-like processes, like abdominal gills in
aquaticnymphsorprolegsofdifferentendopterygoteinsectlarvae,wereregardedasderivatives
ofappendageanlagen(Bitsch,2012;cf.Suzuki&Palopoli,2001).
Although pterygote insects rarely exhibited the extra-abdominal appendages apart from the
genitalia or cerci, most basal insect lineages (Archaeognatha and some Zygentoma) have a
plesiomorphicrichlystructuredabdominalventerbearingthestyliandthecoxaleversiblevesi-
cles,whichwereregardedaselementsofappendicular origin(Bitsch&Bitsch,2004;Klass&
Matushkina,2012).InadultOdonata,abdominalappendage-likestructuresnotassociatedeither
withthegenitaliaorwiththecercihavenotpreviouslybeenfound.
HereIreportpairedabdominal processes(ap)foundinthepleuralregionofabdominal seg-
ments6–9inadultAeshnidaeandsomeotherAnisoptera,whichhasnotpreviouslybeenreported
*Email:[email protected]
(cid:3)c 2016WorldwideDragonflyAssociation
54 N.A.Matushkina
forOdonata.Thesestructureswereobservedincidentallytoabroadcomparativemorphological
investigation of the female postabdomen in Aeshnidae (Odonata, Anisoptera); those observa-
tions led to the focus of this paper. I discuss the origin of ap in a framework of the segment
homologizationbasingonthetransformationofabdominalsegmentsduringmetamorphosis.
Materialandmethods
Thirty-twoadultfemalesof24speciesofOdonatawereinvestigated,includingsixspecimensof
threespeciesofZygoptera,onespecimenofEpiophlebiidae,and25specimensof20speciesof
Anisoptera (Table 1). Aeshnidae were chosen as a focus-group of this research for the reasons
mentionedintheIntroduction.Representativesofotherdragonflyfamilies,twofullydeveloped
finallarvaeofAnaximperator,andonefullydevelopedlarvaofAeshnacyaneawerestudiedto
testsomehypothesesofdevelopmentaloriginofap.
All materials were first examined with a light microscope and then with a scanning elec-
tronmicroscope.Forlightmicroscopy,theabdomensweredissecteddorsolaterally,soakedwith
c.10% water solution of lactic acid for 6–12 h to soften the cuticle (for dried specimens only),
washed in water and macerated for 10–12 h at room temperature with 10% KOH. The macer-
ated abdomens were thoroughly washed in distilled water and examined under glycerin with a
stereo-microscope (Leica M205 C, Leica Microsystems, Museum of Zoology, Natural History
SenckenbergCollectionsDresden,Germany).Forscanningelectronmicroscopy,thecuticleparts
werewashedindistilledwater,dehydratedinagradedethanolseriesandacetone,anddriedatthe
criticalpoint(OMCPD7501).Thencuticlepartsweremountedonastub,sputteredwithgold-
palladium(OM-SC7640)andexaminedwithaZeissEVO-50SEM(Zeiss,MuseumofZoology,
NaturalHistorySenckenbergCollectionsDresden,Germany).
The terminologies of Klass (2008) and Matushkina (2008) were used for the abdominal
skeletonofthedragonflies.
Results
Descriptionofextra-abdominalprocesses
TheabdominalsegmentofadultOdonataischaracterizedbyanenlargedtergalregionthatforms
dorsal,lateralandpartoftheventralsegmentwallandbyanarrowedsternalregionthatispartly
coveredbythetergumlaterally.Themembranouspleuralregionisinvaginatedintothebodyand
can be partially exposed during respiration movements. The anterior half of the pleural region
showsthespiracleinallabdominalsegmentsanteriortotheninthsegment.Sternalsclerotization
bearsbilateralcuticularingrowths,theapodemeb(b7inFigure1),whichisanattachmentpoint
forthedorsoventralmuscle(muscle15inKlass,2008;muscledvpinMatushkina,2008).
In pregenital segments ap is situated in the posterior half of the pleural region, behind the
spiracle,equallyfarfromthesternalandtergalsclerotizations.Aboutatthelevelofapthesternal
sclerotization usually exhibits the apodeme b flanked by the dorsoventral muscles. Depending
on the species, the position of ap in relation to the apodeme varies to some degree (Figure 1).
Ventralregionsoftheeighthandninthgenitalsegmentsaremodifiedduetolocationofgenitalia.
Sternalsclerotizationoftheeighthsegmentisshorterandwiderascomparedwiththepreceding
segments; the basis of ap 8 is situated closer to the posterior edge of the segment. In ninth
segments, the ventral region is entirely occupied by the ovipositor structures; ap 9 is situated
veryclosetotheposteroventralcorneroftheninthtergite,ontheinnermembraneousfoldingof
thetergite.Asarule,aparecoveredbysurroundingcuticleandarenotvisibleexternally.
Table 1. Materialexaminedinthisstudy,presenceofextra-abdominalappendage-likeprocesses(ap)inadultsandlateralspinesinlarvae.
Presenceofsharp
Numberand lateralspinesin
kindof Presenceofapon larvaon6/7/8/9
Systematicassignment Species preservation 6/7/8/9segment segment*
An.:Ae:Aeshnini AeshnaaffinisVanderLinden,1820 1etf +/+/+/+ (conical) ±/+/+/+
An.:Ae:Aeshnini Aeshnacyanea(Müller,1764) 1etf,1etl +/+/+/+ (conical) ±/+/+/+
An.:Ae:Aeshnini Amphiaeschnaampla(Rambur,1842) 1df –/+/+/–(conical) ?
An.:Ae:Aeshnini Coryphaeschnaadnexa(Hagen,1861) 1df –/+/+/–(vestigial) –/±/±/± (veryslender)
An.:Ae:Aeshnini Rhionaeschnaabsoluta(Calvert,1952) 1df –/+/+/+ (vestigial) ?
An.:Ae:Anactini AnaximperatorLeach,1815 4etf,2etl +/+/+/+ +/+/+/+
An.:Ae:Brachytronini Austroaeschnaunicornis(Martin,1901) 1df –/±/±/– +/+/+/+
An.:Ae:Brachytronini Brachytronpratense(Müller,1764) 1etf ±/±/±/+ ±/+/+/+
An.:Ae:Brachytronini Epiaeschnaheros(Fabricius,1798) 2df ?/ ±/±/± +/+/+/+
AAnn..::AAee::GGoommpphhaaeesscchhnniinnii BBoaysieareiascvhinnaosjaan(aStaay,(S1a8y4,01)840) 21ddff +/+±//+±//–±(w/–el(lcdoenvicealol)ped) ++//++//++//++ ((aallllssttrroonngg)) First
An.:Ae:Gomphaeschnini Gomphaeschnaantilope(Hagen,1874) 1df –/–/+/– +/+/+/+ re
c
AAnn..::AAee::GGoymnapchaanethscahgnininii TGeylnepahcalenbtihaataildlyealardMiCaratminp,i1o9n0i9nTillyard,1916 11ddff –/–±/–//–±/–/– ±+//++//++//++ ordo
An.:Ae:Gynacanthagini Triacanthagynaseptima(SelysinSagra,1857) 1df –/–/±/– ? fe
x
An.:Petaluridae PhenesraptorRambur,1842 1df –/–/–/– –/–/–/– tr
a
An.:Cordulegasteridae CordulegasterbidentataSelys,1843 1etf –/–/–/– –/–/–/– -a
An.:Corduliidae Epithecabimaculata(Charpentier,1825) 1etf –/–/+/+ –/–/+/+ bd
o
An.:Gomphidae Gomphusvulgatissimus(Linnaeus,1758) 1etf –/–/– –/–/–/– m
An.:Libellulidae OrthetrumcancellatumLinnaeus,1758 1etf –/–/±/± –/–/±/± ina
Az:Epiophlebiidae Epiophlebiasuperstes(Sélys,1889) 1etf –/–/–/– –/–/–/– lp
Zyg.:Eupheidae Epallagefatime(Charpentier,1840) 2etf [+/+/+/–](vestiges) [+/+/+/–](gills) roc
Zyg.:Calopterygidae Hetaerinaamericana(Fabricius,1798) 3etf –/–/–/– –/–/–/+ es
s
Zyg.:Coenagrionidae Coenagrionpulchellum(VanderLinden,1825) 1etf –/–/–/– –/–/–/– es
in
*Basedonliteraturedataandunpublishedobservations.Abbreviations:et,inethanol;d,dry;f,female;l,finallarva;An.,Anisoptera;Ae.,Aeshnidae;Az.,Anisozygoptera;Zyg.,Zygoptera; +,large; ±,medium, ad
–,smallorabsent;[...],presenceoflarvalgillsandtheirvestiges;?,informationabsent. ult
O
d
o
n
a
ta
5
5
56 N.A.Matushkina
Figure 1. Varietyofappendage-likeprocessesinfemalesofAnaximperator,lightmicroscopy:(a)maceratedseventh
segmentventrally;(b)non-maceratedeighthsegmentventrallywithinsetenlargedin(d);(c–e)morphologicalvariability
ofappendage-likeprocesses.ap7,ap8,ap9,processesonpleuralareaofseventh,eighthandninthsegmentwall,respec-
tively;b7,postspiracularapodemeonseventhsternum;p,posteriordirection;si7,spiracleofseventhsegment;“ST7”,
“ST8”,seventhandeighthsternums,respectively(forscleritecompositionofsternumindragonfliesseeKlass2008);
TG7,TG8,TG9,seventh,eighthandninthtergites,respectively.Emptyarrowheadindicatesproximalendofprocessap.
Scalebars:(a),(b)0.001mm;(c–e)0.2mm.
Eachapisahollowunsegmentedoutgrowthofthebodywallwithoutintrinsicmusclesortra-
cheation.OnenewlyemergedspecimenofAnaximperatorwasfoundtobearthemostprominent
ap(upto1mmlong),whichcanbeeasilyvisibleexternally.Eachapconsistsofanarrowneck-
likestalkwithdelicatemembranouswallextendingtoastiffsclerotizedandmelanizedsharply
pointed rod (Figures 1a, c, 2c, e). Similarly structured ap were found on the ninth segment in
A. parthenope. Presence of the stalk implies these ap might be highly movable. Other teneral
specimensofAnaximperatorbearaweaklysclerotizedworm-likeap8ofc.350–400mkmlong
(Figure1b,d).Mostusually,apisrepresentedbyaweaklysclerotizedconicaloutgrowthwithout
evidentwaist(Figure2b).Thebaseofapsclerotizationmayhaveacomplexshapewithoutclear
margins, whereas the tip of ap is usually curved posteriorly. In Epiaeschna heros, a short ap8
Firstrecordofextra-abdominalprocessesinadultOdonata 57
(a) (b) (c)
(d) (e)
(f) (g)
Figure 2. Comparisonofvestigiallarvalgillbyscanningelectronmicroscopyin(a)femaleEpallagefatima(Euphaei-
dae); and (b–g) appendage-like processes in females of Aeshnidae: (b) Aeshna affinis; (c, e) Anax imperator; (d)
Brachytronpratense;(f,g)Epiaeschnaheros.TG8,TG9,eighthandninthtergites,respectively;ap8,ap9,processes
onpleuralareaofeighthandninthsegmentwall,respectively.Emptyarrowheadindicatesvestigeoflarvalgill.Dou-
blearrowindicateslateral(l)andposterior(p)directions.Scalebars:(a),(c),(e)0.1mm;(b)0.3mm;(d)0.05mm;
(f)0.02mm;(g)0.001mm.
showsaregularapicalsculpture(Figure2f,g).Severalspecimensbearaverysmallmembrane-
ous ap in the form of a nipple-shaped or finger-shaped protuberance or a bulge (Figure 1e). In
caseofitsmaximalreduction,apappearsasaswollenregionofpleuralmembrane.
Fully developed or vestigial ap were found in all representatives of Aeshnidae on seventh–
ninth abdominal segments (less often on seventh and eighth segments or on sixth–ninth
segments) (see Table 1). In Basiaeshna janata ap were detected on fifth–eighth abdominal
segments. Among other Odonata studied here, ap was found in Epitheca bimaculata (Corduli-
idae) and Orthetrum cancellatum (Libellulidae). Age of imago, its body size and degree of
58 N.A.Matushkina
sclerotization, taxonomic affiliation of the specimen and position on the abdomen apparently
donotaffectthemorphologyofap.
Correspondencewithlarvallateralspines
Aeshnidlarvaearecharacterizedbyprominentlateralspinesontheposteriorhalfoftheabdomen
(Table 1). These spines are very large, sharply pointed outgrowths of the lateral edge of 5–9
tergiteswhicharegraduallyenlargedinsubsequentsegments.Theregionbearingthespineisnot
separatedfromtheremainingtergitewall.Thepleuralregioninafinalinstarlarvaconsistsoftwo
wellsclerotizedplates–thetriangularanterolateralone,PLa,andtheposteriorone,PLp(Figure
3a,d).Unlikeinprecedingsegments,PLa8isverysmallandPLp8showsacleartransverserow
ofdenticlesthatlaterallyendsatthelateralspine.PLpbearstheremnantofthespiracle“si”asa
darkwell-borderedpatchsituatedinitsanteriorregion.Inthestudiedfinallarvaewithdeveloped
imaginal cuticle under the larval cuticle, the larval spine represents a mostly empty outgrowth
bearing only a small soft, pale ap inside (Figure 3a–c). In the imago, instead of the firm larval
pleuralplatesthereisamostlymembraneousarea(Figure3d,e).Thus,themembranesituated
betweenthetergiteTGandsterniteSTofanabdominalsegmentbearsintheimagotwoevident
structures–thespiraclesiandtheabdominalprocessap(Figure3e).
Comparisonwithvestigesoflarvalgills
Euphaeidae and Polythoridae are only recent Odonata with supplementary larval gills running
downthesidesoftheabdomen(Lok&Orr,2009).InEpallagefatime(Zygoptera,Euphaeidae),
thegillisamovablegrub-likehollowappendagewithintrinsictracheationandonemusclecon-
nectingthegillbasewiththerespectivetergite;thusthegillsaremovableandfunctionallyloaded
appendages.Thegillsareattachedtothepleuralregionofabdominalsegments2–8bilaterally,
just below the tergite and behind the spiracle vestige (Kluge, 2000). My investigation of adult
Epallageshownthatgillsdisappeartoasmallvestigeintheformofamembranousconvexityat
theventroposterioredgeoftergites2–8(Figure2a).IfcomparedwiththegillvestigesinEpal-
lage,examinedapareasarulemoredevelopedstructures,whichbearhairs,sclerotizations,and,
asarule,exhibitadefiniteshape.Topographically,apandgillvestigesinEpallagearesimilar.
Discussion
Pairedextra-abdominalprocesses(ap)arefoundinthepleuralregionofthesixthtoninth(rarely
fifthtoninth)abdominalsegmentsinseveraladultAnisopteraspecies.Mystudyoffinalinstar
larvaeshowthattheimaginalaparedevelopingunderthecuticleoflarvallateralspines,which
occupytheposterolateralareasofthelarvaltergite.Thisfactleadstotheassertionthatthepleural
region in adult abdominal segments of examined Odonata species corresponds topographically
tothelarvalpleuriteandtoapartofthelarvaltergite.Consequently,theimaginalpleuralregion
intheabdomenofAeshnidaeisofacomplexpleuro-tergalorigin(cf.Matushkina,2008).
WhyapareappearinginadultAnisoptera,andwhethertheyareofanyfunctionalimportance,
isanobscurematter.Larvalaeshniddragonfliesareaquaticpredators.Experimentsprovideevi-
dencethatspinesofananisopteranlarvamayserveasadefencetoolagainstpredatorslikefishes
(Johansson&Samuelson,1994;Mikolajewski&Johansson,2004).However,spinesmightalso
beadaptationstootherfactors,suchaskeepingthelarvaefromsinkingintothebottomsubstrate
(Corbet,1957)orhelpingthemtoclingtovegetation(Aguiar,1989).InOdonata,metamorphosis
leadstodrasticmorphologicalmodificationsassociatedwiththehabitatshiftfromaquaticlarvae
Firstrecordofextra-abdominalprocessesinadultOdonata 59
(a) (b) (c)
(d) (e)
Figure 3. VentralaspectsoftheeighthandninthabdominalsegmentinAeshnidae,righthalfshownonly,(a–c)light
microscopy,(d–e)diagrammatically.(a)TheeighthabdominalsegmentoffinallarvaofAeshnacyaneaanditsimaginal
cuticleunderlyingthelarvalcuticle(b);(c)imaginalcuticleunderlyingthelarvalcuticleoftheninthabdominalsegment
offinallarvaofAeshnacyanea;(d),(e)ventralaspectsoftheeighthsegmentinfinallarva(d)andfemale(e)ofAnax
imperator.Segmentwallin(e)isquasibentventrallyandstraightened.ap8,“ap8”,appendage-likeprocessandlateral
spine on tergite to which it is assumedly homologous, respectively; b8, postspiracular apodeme of eighth segment;
PLa8,PLp8,anteriorandposteriorpartsofpleurite,respectively;“ST8”,sternalsclerotization(forargumentsforits
complexoriginseeKlass2008);si8,“si8”,spiraclesclerotizationanditsanlageonlarvalpleurite,respectively;TG8,
eighthtergite.Greyscalesin(d)and(e)indicatedifferentdegreeofsclerotization.Doublearrowindicateslateral(l)and
posterior(p)directions.Scalebars:(a–c)0.5mm;(d)and(e)0.001mm.
to aerial adults (e.g. Leipelt, Suhling, & Gorb, 2010). Specifically in Aeshnidae, the abdomen
becomes longer and slender, its tergites are enlarged and swollen and sternites are narrowed
(Asahina,1954).Whedon(1929)assertsthatchangeoftheshapeoftheabdomeninOdonatais
apparentlycausedbychangeofrespirationandlocomotionmode.Inaeshnidlarvae,theabdomen
ventilationmovementsconsistofarhythmicraisingandloweringoftheposteriorabdominalven-
ters(whichincludethesterniteandpleuralregions)againsttheterga;whereinthewholepleural
regionremainsexposedduringtheventilationcycle(Mill&Pickard,1972).Incontrast,theven-
tilationmovementsintheadultabdomenconsistofalternatepullingofthenarrowsternitedeep
inside the swollen tergite and subsequent protrusion of the sternite to its starting position; the
60 N.A.Matushkina
whole pleural region, including the area of ap, remains mostly hidden within the segment all
the time. Therefore, ap remains deep in a slit between the abdominal tergite and sternite. This
positionmakesunlikelyanysuggestioneitherontheexteroceptiveordefencefunctionofap.
Onthebasisoftheavailabledata,Iaminclinedtoconsiderthattheaparerathervestigesof
firmlarvalspinesthatareretainedinanimago.Indeed,thebodyofthefreshlyemergedimago
in Odonata has several non-functional larval traits, especially in the musculature (Matushkina,
2008; Whedon, 1929), which may persist in the mature imago. However, virtually no infor-
mation has previously been available on the changes undergone by peculiar outgrowths of the
larval body wall, like prongs or spurs, in the metamorphosis to an imago. Further evidence in
favourofresidualnon-functionaloriginofapislackofanytracesofinnervationandmuscula-
tureassociatedwithap,andessentialvariabilityoftheshapeanddegreeofsclerotizationofap
amongspecimensofthesamespecies.Apeculiarlystructuredapicalsurfaceofaprecordedfrom
Epiaeschnaherosremainsobscure.
Ifmyspeculationaboutthenon-functionaloriginofthefoundprocessesistrue,itisunclear
whyAeshnidaeexhibitmuchmoredevelopedvestigesoflarvalspines(ap)ascomparedtothe
other dragonfly lineages studied, and as compared to diminutive vestiges of the larval gills in
Euphaeidae.Perhapsthesizeanddegreeofsclerotizationmayaffectthedisappearanceofcutic-
ularstructuresduringmetamorphosisinsomespecificway.Ifso,verylargedragonfliessuchas
Aeshnidaehaveabetterchancetoretainfirm,well-sclerotizedlarvalcuticularstructuresinthe
imago.Theseissuesrequirefurtherinvestigationinordertodeepenourfundamentalknowledge
abouttheinsectbodymodificationinthemetamorphosisandthemechanismoftheheterochronic
developmentintheinsects.
Acknowledgements
IwouldliketothankAlexMartynov,SergejMartynov,AlexGumovsky,FrankLouisCarle,NataliavonEllenriederand
R.W.Garrisonfordonationsofspecimens,andRoyJ.BeckemeyerandMikeMayforlinguistichelp.Iamgratefulto
SebastianBüsseandananonymousreviewerforcriticalreviewingofthemanuscript.
Funding
TheresearchwaspartlysupportedbytheDAADunderGrant322/or-eandbytheSenckenbergInstitutionunderGrant
forInvitedResearches2015.
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